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Species in Sect. Alatae from Luzon, Philippines Showing Striking Pitcher Convergence with N

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Species in Sect. Alatae from Luzon, Philippines Showing Striking Pitcher Convergence with N Nepenthes maximoides (Nepenthaceae) a new, critically endangered (possibly extinct) species in Sect. Alatae from Luzon, Philippines showing striking pitcher convergence with N. maxima (Sect. Regiae) of Indonesia Charles King and Martin Cheek Science, Royal Botanic Gardens, Kew, Richmond, UK ABSTRACT Nepenthes maximoides sp. nov. (Sect. Alatae) is described and assessed as Critically Endangered (Possibly Extinct) from Luzon, Philippines and appears unrecorded in 110 years. The spectacular, large, narrowly funnel-shaped upper pitchers, lids with recurved basal and filiform apical appendages, unlike any other species in the Philippines, closely resemble those of N. maxima (Sect. Regiae) of Sulawesi–New Guinea, likely due to convergent evolution. Following recent phylogenomic analysis, sect. Alatae is divided into two, Sect. Alatae sensu stricto of Luzon to Sibuyan (including N. maximoides), and Sect. Micramphorae, expanded and recircumscribed to encompass those species of the southern Visayas, and Mindanao. A key is provided to the six species now recognised in the newly narrowly recircumscribed Sect. Alatae. The number of Nepenthes species recorded from Luzon has increased from two in 2001, to eight in 2020, all but one of which are endemic to that island, and four of which appear to be point endemics. Subjects Biodiversity, Conservation Biology, Plant Science, Taxonomy Submitted 16 July 2020 Keywords Mt Banahaw, Extinct, Tayabas province, Conservation, H.M. Curran, Systematics, Accepted 17 August 2020 Published 11 September 2020 Taxonomy Corresponding author INTRODUCTION Martin Cheek, [email protected] This paper is one in a series leading to a monograph of the genus Nepenthes building on a Academic editor David Roberts skeletal revision of the genus (Jebb & Cheek, 1997) and the account for Flora Malesiana Additional Information and (Cheek & Jebb, 2001). While in 2001 only 85 species were accepted for the genus, today Declarations can be found on the figure lies at 181 (Murphy et al., 2020). In 2001 the geographic units with highest page 15 Nepenthes species diversity were Sumatra and Borneo, each with over 30 species, while DOI 10.7717/peerj.9899 just 12 species were recorded for the Philippines (Cheek & Jebb, 2001). However, since Copyright then the Philippines has dominated for discovery of new species. In 2013 alone, twelve 2020 King and Cheek new species were published from the Philippines (Cheek & Jebb, 2013a, 2013b, 2013c, Distributed under Creative Commons CC-BY 4.0 2013d, 2013e, 2013f, 2013g; Micheler et al., 2013), and new species continue to be added every year (Cheek & Jebb, 2014; Cheek, Tandang & Pelser, 2015; Gronemeyer et al., 2016; How to cite this article King C, Cheek M. 2020. Nepenthes maximoides (Nepenthaceae) a new, critically endangered (possibly extinct) species in Sect. Alatae from Luzon, Philippines showing striking pitcher convergence with N. maxima (Sect. Regiae) of Indonesia. PeerJ 8:e9899 DOI 10.7717/peerj.9899 Figure 1 Nepenthes maximoides Cheek. Photo of the type specimen Curran s.n. (Univ. Pennsylvania sheet 70707), PH. Note that material is mounted pitchers facing downward. Photo by Martin Cheek. Full-size DOI: 10.7717/peerj.9899/fig-1 Lagunday et al., 2017; Amoroso et al., 2018; Robinson, Zamudio & Caballero, 2019a). The current total of Nepenthes species for the Philippines is 59 (Pelser, Barcelona & Nickrent, 2011 onwards, accessed May 2020) now far exceeding the totals for other phytogeographic units such as Sumatra and Borneo. However, new species of Nepenthes continue to be discovered elsewhere in SE Asia, from Indonesia, with new species described from Halmahera (Cheek, 2015), Sulawesi (Cheek & Jebb, 2016a, 2016b) and New Guinea (Cheek et al., 2018), and also from Malaysia, with new species from Borneo (Robinson et al., 2019b; Golos et al., 2020). During a study of specimens of Nepenthes from the Philippines, one specimen, Curran s.n.(Fig. 1), previously determined as N. alata Blanco (in fact N. graciliflora Elmer (Cheek & Jebb, 2013g)), was initially set aside since it seemed to have been mislabelled as King and Cheek (2020), PeerJ, DOI 10.7717/peerj.9899 2/19 from Luzon when in fact the specimen appeared to be Nepenthes maxima Nees, a widespread and variable species occurring from Sulawesi to New Guinea but absent from Philippines (Cheek & Jebb, 2001). Nepenthes maxima is distinctive for its narrowly funnel-shaped upper pitchers, flattened peristome with undulate outer margin, large, ovate-elliptic lid, a usually hooked basal appendage and a filiform apical lid appendage (Cheek & Jebb, 2001). No known species in the Philippines remotely resembles it. Nepenthes maxima (Borneo-New Guinea) is placed in Sect. Regiae Danser which is entirely absent from Philippines (Cheek & Jebb, 2015). However, a second inspection of Curran s.n. showed that features of the stem and petiole, in contrast to the pitchers, are not those of sect. Regiae Danser (Danser, 1928), but instead are consistent with those of Sect. Alatae Jebb & Cheek, which as currently defined is endemic to the Philippines, occurring from Luzon to Mindanao (Cheek & Jebb, 2015). Curran s.n. has petioles with conspicuous, patent wings (T-shaped in transverse section) while those of Sect. Regiae are inconspicuous or erect (U-shaped in transverse section); the axillary buds are inconspicuous and the indumentum of stem and leaf-blades is absent or inconspicuous (in Sect. Regiae the axillary buds are conspicuous, several mm long, and spike-like; and the indumentum is robust, branched, brown and present at least at the stem apex). In Sect. Alatae moreover, the phyllotaxy is spiral and not, as in Regiae, distichous (Danser, 1928; Cheek & Jebb, 2015). It seems clear that Curran s.n. might have been correctly labelled as a Philippine species, after all. In this article we key out Curran s.n., distinguishing it from all other species of Sect. Alatae in northern Philippines (Luzon and the northern Visayas) describing it as Nepenthes maximoides Cheek, diagnosing it from N. graciliflora which it had previously been identified as. We also compare it with N. copelandii Macfarl. of Mindanao which unusually also shares the narrowly funneliform upper pitcher shape. We present biographical notes on the collector and deduce the location of the geographic source of his collection, likely Mount Banahaw, and consider the likelihood of the extinction of this species. We consider the presence of terminal lid appendages in the genus and their homology; we also discuss morphological convergence with N. maxima. Finally, we discuss the division and new, narrow recircumscription of Sect. Alatae based on new phylogenomic data. MATERIALS AND METHODS The specimen on which this paper is centred is on loan from PH and was compared with material presently at K including that on loan from A, BISH, BRIT, CAS, GH, L, NY, US and that studied at BO by the second author. The electronic version of this article in Portable Document Format (PDF) will represent a published work according to the International Code of Nomenclature for algae, fungi and plants (ICN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone. In addition, new names contained in this work which have been issued with identifiers by IPNI will eventually be made available to the Global Names Index. The IPNI LSIDs can be resolved and the associated information viewed through any standard web browser by appending King and Cheek (2020), PeerJ, DOI 10.7717/peerj.9899 3/19 the LSID contained in this publication to the prefix http://ipni.org/. The online version of this work is archived and available from the following digital repositories: PeerJ, PubMed Central, and CLOCKSS. Herbarium citations follow Index Herbariorum (Thiers, 2020) and binomial authorities the International Plant Names Index (IPNI, 2020). The conservation assessment was made using the categories and criteria of IUCN (2012). Herbarium material was examined with a Leica Wild M8 dissecting binocular microscope fitted with an eyepiece graticule measuring in units of 0.025 mm at maximum magnification. The drawing was made with the same equipment using Leica 308700 camera lucida attachment. The specimen was partly unmounted to expose the characters needed to first identify and second characterise the species. It had originally been mounted with the lower surface of the lid face down, obscuring critical features. The map was made using SimpleMappr (https://www.simplemappr.net). Information on the likely location of the collection was gathered by analysing other herbarium specimens collected by H.M. Curran recorded on JStor Global Plants (2020). RESULTS TAXONOMIC TREATMENT Key to the species of Nepenthes sect. Alatae in Luzon and northern Visayas 1 Monopodial erect shrublets 30 cm tall (including inflorescence), climbing stems and upper pitchers always absent; lower pitchers with column extending onto lower surface of the lid; lid lower surface lacking appendages. Sibuyan .......N. argentii Jebb & Cheek 1 Climbers exceeding 1 m tall (where known), climbing stems and upper pitchers present at maturity; pitchers with column usually absent, if present, not extending onto lower surface of the lid; lid lower surface with basal appendage (except N. armin).........2 2 Upper pitchers narrowly infundibulate, broadest at the peristome; lower surface of lid with both basal and apical appendage. Luzon . ...............N. maximoides Cheek 2 Upper pitchers ovoid-cylindric, broadest in the basal
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